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International Scholarly Research NetworkISRN RehabilitationVolume 2012, Article ID 402612, 7 pagesdoi:10.5402/2012/402612

Research Article

Proprioceptive Neuromuscular Facilitation Improves Balanceand Knee Extensors Strength of Older Fallers

Marcelo Pinto Pereira1 and Mauro Goncalves2

1 Posture and Gait Studies Laboratory, Physical Education Department, Bioscience Institute,Universidade Estadual Paulista at Rio Claro, Avenida 24A, 1515, 13506-900 Rio Claro, SP, Brazil

2 Biomechanics Laboratory, Physical Education Department, Bioscience Institute, Universidade Estadual Paulista at Rio Claro,Avenida 24A, 1515, 13506-900 Rio Claro, SP, Brazil

Correspondence should be addressed to Marcelo Pinto Pereira, [email protected]

Received 7 September 2012; Accepted 4 October 2012

Academic Editors: Y. Hu, M. Syczewska, and S. P. Tokmakidis

Copyright © 2012 M. P. Pereira and M. Goncalves. This is an open access article distributed under the Creative CommonsAttribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work isproperly cited.

Falls are one of the major problems for elderly people and proprioceptive exercises have been suggested as an alternative in reha-bilitation and preventive programs. The purpose of this study was to investigate the influence of a proprioceptive neuromuscularfacilitation (PNF) exercise program on balance, knee extension and flexion isometric torque, and knee extension rate of forcedevelopment (RFD). Fourteen older faller subjects (>60 years) were equally assigned into two groups: a control group (CG: n = 7)and a training group (TG: n = 7). The PNF training program was performed for 10 weeks on TG, with a frequency of three timesper week. Patients were assessed before and after the PNF program, with respect to balance (Berg Balance Scale score—BBS), kneemaximal isometric extension and flexion torque, knee extensor RFD, and knee extensors and flexors neuromuscular activationlevel and coactivation level around the knee. After 10 weeks, balance (P < 0.001) and knee extension torque (P = 0.05) wereimproved in TG while no differences were found for CG. These improvements were mainly attributed to central nervous systemadaptations, since no differences were found for neuromuscular activation level and coactivation.

1. Introduction

Falls in elderly are associated to both mortality and morbidlyincreasing. Falls are also the major death cause in peopleaging over 85 years [1]. Many tools were used to discriminatepeople on fall risk in the past. However, the most used by itslow cost is the Berg Balance Scale [2, 3]. According to Lajoieand Gallapher [3] scores lower than or equal to 46 on BergBalance Scale (BBS) classify subjects as fallers with 93% ofspecificity.

Strength reduction is pointed as the major cause of fallsin this population [4] and, therefore, maximal torque shouldbe accessed on daily-life clinical tests. The center of massor center of pressure dislocation and velocity are useful todiscriminate subjects on fall risk [5]. However, these testsrequire expensive equipment and high advance knowledge.This problem is not observed on isometric contractionstests, where both the strength level and the quality of power

production can be observed. This latter aspect had beenstudied by means of rate of force development [6–10].

Lower torque and power production on elderly fallers isassociated with an increased coactivation around knee andankle [1, 11]. Coactivation, defined as the simultaneous mus-cle contraction around a joint [12], had also being pointed asresponsible to reduced walking speed and increase fall risk ofelderly [13–15].

Beyond all exercise programs proposed to reduce fall riskin this population, proprioceptive neuromuscular facilitation(PNF) technique is presented as an interesting choice, since,according to Lee and Kerrigan [15], exercise programs withobjective to enhance balance on elderly should involve coor-dination and proprioception activities and not only strength-en exercises [8, 16]. During the PNF movement execution,muscles are briefly stretched before contraction, excitingneuromuscular endings which produce higher levels of force[17, 18]. Also, the movements in PNF are executed in

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diagonal pattern that is parallel to muscular topography,which reproduces physiological movements, as gait [17, 18].It was also suggested that a higher balance between agonisticand antagonistic muscles activation is achieved after PNFexercises [17, 18] reducing coactivation. However, the effectsof a PNF training program on fall risk in older people are stillunknown.

The aim of this study was to evaluate the effects of aPNF exercise program on elderly on fall risk and to evaluatethe neuromuscular and isometric performance response tothis exercise program. As hypothesis, it is believed that bothfall risk and isometric torque will be improved after trainingand that coactivation around knee will be reduced, sincehigher balance between agonistic and antagonistic musclesactivation is achieved after PNF exercises.

2. Material and Methods

2.1. Subjects. Older community subjects were personallyinvited to participate in this study. They were only evaluatedafter signing an informed consent approved by Local EthicsCommittee. As inclusion criteria, all subjects should be olderthan 60 years, considered as inactive-score lower or equalthan 9.4 at Modified Baecke Questionnaire for older people[19] and on fall risk score of 46 or less on Berg Balance Scale[3]. Exclusion criteria were the presence of any orthopedic,cardiovascular, vestibular, psychiatric, neurological, and anyother condition that would not allow the execution of allstudy tasks. A total of 940 subjects were invited to participate;however, only 142 subjects proposed to be evaluated. After ahealthy questionnaire and inclusion and exclusion criteria,only 16 women were able to perform all the proposed tasksand met the inclusion criteria. They were randomly assignedin two groups: a training group (TG) and a control group(CG). One patient in each group failed to complete theoutcome measures and both were, therefore, excluded fromthe study (Figure 1).

2.2. Experimental Design. Volunteers on both groups wereevaluated before (pre-) and after (post-) PNF program. Atthe first day, after the Berg Balance Scale (BBS) application[3], volunteers answered a physical activity level and ahealth questionnaire. If they were eligible to participate, theyreturned to the laboratory on a second day (within 48 hoursfrom the first visit). After the PNF program, data collectionwas not conducted more than one week apart from the lasttraining session.

2.3. Training Program. PNF exercise program consisted ofthree sessions per week for a period of ten weeks, and eachsession was not apart from one another more than two days.Each session lasted about 90 minutes whereas eight differentmovement patterns (Table 1) were used—they were executedon both limbs. The same physiotherapist (appropriatelyinstructed) conducted all training sessions where maximalmanual resistance were applied; the resistance progressiontrough the 10 weeks was carried out according to PNF prin-ciples [20]. Also, five different training stages adapted from

Total subjects invited

Refused participation

Total number of health questionnaire and BergBalance Scale application

n = 142

Not met health conditionsor inclusion criteria

Total number of subjects enrolledn = 16

Random assignedTraining group

(TG)n = 8

Control group (CG)

n = 8

Outcome data:10 weeksn = 7

Outcome data:10 weeksn = 7

Loses (n = 1) each group

Reason: loss of interest

N = 940

Figure 1: Study flow diagram.

Voss et al. [20] were conducted—(i) rhythmic initiation:patterns are executed in a progressive manner through pas-sive, assisted and active movements (conducted in two initialsessions); (ii) dynamic reversion: patient moves limb isoton-ically through resistance following agonistic and antagonisticpatterns (performed from third session to fifth trainingweek: three series with five repetitions of each pattern, withone-minute rest interval between series and three minutesbetween movement patterns); (iii) isotonic combination:patient executes the agonistic movement, resist isometricallyat the movement end and returns to initial position eccentri-cally (executed from the sixth to ninth week: two series withfive repetition of each pattern, with one minute rest periodbetween repetitions and two minutes between movements[17]; (iv) rhythmic stabilization: isometric contraction ofagonist pattern followed by antagonist isometric contraction(executed on the ninth and tenth weeks, since it is the leasteffective technique [21]).

Stretching exercises were conducted immediately afterthe strengthen session on both limbs and were repeated fromthe second day until the last session. Contract-relax (weeksfrom one to five) and maintain-relax (weeks six to ten) tech-niques were used and all movement patterns described beforewere performed. Contract-relax stretch application beganwith the physiotherapist passively positioning the lower limbon the desired movement pattern in maximal stretchingwithout pain (the position where an “end feel” was notedby the physiotherapist). When this position was attained, thesubject was instructed to perform the antagonist movementpattern with maximal force against the physiotherapist man-ual restriction (a brief rotational movement was allowed).After five seconds, subject was instructed to completely relaxthe musculature while the physiotherapist passively movedthe limb to a new maximal stretch position maintainedfor 15 seconds. The same procedures were adopted inmaintain-relax; however, the physiotherapist did not allow

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Table 1: Strengthening movement patterns.

Initial position Final position

D1-fl H extension, abduction, and internal rotation; K flexion;A flexion and eversion; F flexion and adduction

H flexion, adduction, and external rotation; K extension;A dorsiflexion and inversion; F extension and abduction

D2-fl H extension, abduction, and internal rotation; K extension;A flexion and eversion; F flexion and adduction

H flexion, adduction, and external rotation; K flexion;A dorsiflexion and inversion; F extension and abduction

D3-fl H extension, abduction, and internal rotation; K flexion;A flexion and inversion; F flexion and abduction

H flexion, adduction, and external rotation; K extension;A extension and eversion; F extension and adduction

D4-fl H extension, abduction, and internal rotation; K extension;A flexion and inversion; F flexion and abduction

H flexion, adduction, and external rotation; K flexion;A dorsiflexion and eversion; F extension and adduction

D1-ext H flexion, adduction, and external rotation; K flexion;A dorsiflexion and inversion; F extension and abduction

H extension, abduction, and internal rotation; K extension;A flexion and eversion; F flexion and adduction

D2-ext H flexion, adduction, and external rotation; K extension;A dorsiflexion and inversion; F extension and abduction

H extension, abduction, and internal rotation; K flexion;A flexion and eversion; F flexion and adduction

D3-ext H flexion, abduction, and internal rotation; K flexion;A dorsiflexion and eversion; F flexion and abduction

H extension, adduction, and external rotation; K extension;A flexion and inversion; F extension and adduction

D4-ext H flexion, abduction, and internal rotation; K extension;A dorsiflexion and eversion; F flexion and abduction

H extension, adduction, and external rotation; K flexion;A flexion and inversion; F extension and adduction

H (hip); K (knee); A (ankle); F (feet fingers); fl (flexion); ext (extension).

any rotational movement on the contraction phase. The totalstretching volume was composed by four series of 20 secondfor each movement pattern [22, 23].

The subjects in the CG continued their normal routineand were encouraged to maintain an active lifestyle. Theexaminer continued to maintain contact with the subjectsduring all study period.

2.4. Data Recording. Volunteers were positioned in a seatedposture with hip and knees flexed at 90 degrees and ankle andspine in neutral position. A load cell (EMG System) was usedto achieve the isometric knee extension and flexion torque,which were both fixed on the volunteer’s right ankle andon a metal bar positioned perpendicularly to ground. Afterthree submaximal contractions (self-selected submaximalforce level) to familiarization, and three knee extension andflexion (in a random order) maximal voluntary contractionswere performed, with five seconds long and five minutes restbetween them. Volunteers received instructions to performthe maximal strength as quickly as possible. Force data werecollected using a sample rate of 1.000 Hz.

Circular passive bipolar Ag/AgCl electrodes with 1cmdiameter of effective caption area were positioned overthe vastus lateralis (VL), vastus medialis (VM), and rectusfemoris (RF) and biceps femoris (BF) after shaving, abrasionand skin cleaning according to the SENIAM standard recom-mendations. Muscle activity was recorded at 1.000 Hz with afour-channel telemetric system (Telemyo 900-Noraxon) witha 10 to 500 Hz bandwidth and 1.000x gain.

2.5. Data Processing. The analyses were conducted usingspecific algorithms developed in MatLab. All force andelectromyography variables were achieved from the trial withmaximal isometric force production (maximal voluntary

contraction—MVC). Rates of force development (RFD)were determined as the slope between time and force(Δmoment/Δtime) over time intervals of 0–0.50, 0–0.10, and0–0.20 seconds [10] relative to the force production onset(defined as 10% MVC [7, 9]).

The EMG root mean square was achieved from thesecond that presented the least variation in the load-celldata both at knee extension and flexion contractions. Thisone-second period was chosen by visual inspection and itslocation varied among the total five seconds period (i.e.,in the first contraction, the one-second period chosen was2.8-3.8 seconds and in the next contraction it was 1.5-2.5seconds).

Coactivation Index (CCI) was determined according tothe following formula [11, 14]:

CCI = BFExe

× 100, (1)

where BF is the BF EMG activity (RMS) and Exe is theknee extensor (VL, RF, and VM mean) EMG activity, bothobtained during knee extension contraction.

2.6. Statistical Analyze. After distribution test (Shapiro-Wilk test) the following procedures were conducted on theStatistica 7.0 software: to determine groups influence onbaseline anthropometric and baseline data a Student-t testfor independent variables were used; to determine the PNFprogram effect on EMG, force data, and on each BBS activityand total score, paired t-tests were performed. A P value of0.05 was considered statistically significant.

3. Results

Both groups presented similar age (72.71± 6.82 and 71.71±6.63 years for CG and TG), height (1.55 m ± 0.48 and


Table 2: Mean (1 SD) Berg Balance Scale (arbitrary units) by task and total for training group (TG) and control group (CG) pre- andpost-training period.

TG CG

Before After Before After

Sitting to standing 3.29 (0.49) 3.14 (0.38) 3.14 (0.38) 3.29 (0.49)

Standing unsupported 4.00 (0.00) 4.00 (0.00) 4.00 (0.00) 4.00 (0.00)

Sitting unsupported 4.00 (0.00) 4.00 (0.00) 4.00 (0.00) 4.00 (0.00)

Standing to sitting 2.00 (0.00) 3.00∗ (0.82) 2.43 (0.53) 2.29 (0.49)

Transfers 3.43 (0.53) 3.29 (0.49) 3.00 (0.00) 3.00 (0.00)

Standing with eyes closed 3.71 (0.49) 3.71 (0.49) 3.71 (0.49) 3.86 (0.38)

Standing with feet together 3.43 (0.53) 4.00∗ (0.00) 3.71 (0.49) 3.86 (0.38)

Reaching forward with outstretched arm 3.43 (0.53) 4.00∗ (0.00) 3.57 (0.53) 3.43 (0.53)

Retrieving object from floor 3.71 (0.49) 4.00 (0.00) 3.86 (0.38) 4.00 (0.00)

Turning to look behind 3.14 (0.90) 3.57 (0.79) 2.29 (0.49) 2.71 (0.76)

Turning 360 degrees 2.71 (0.76) 3.57 (0.79) 2.71 (1.11) 3.57 (0.53)

Placing alternate foot on stool 3.43 (0.79) 3.86 (0.38) 2.86 (1.07) 3.43 (0.53)

Standing with one foot in front 2.14 (0.38) 3.29∗ (0.49) 2.29 (1.11) 2.29 (1.25)

Standing on one foot 1.86 (1.07) 2.43 (0.53) 2.14 (1.07) 1.43 (0.98)

Total score 44.29 (1.60) 52.71∗∗ (1.60) 43.71 (2.36) 45.14 (2.12)∗P < 0.03 on paired student t-test.∗∗P < 0.01 on paired student t-test.

Table 3: Force means (1 SD) values by group and test.

TG CG

Before After P value Before After P value

RFD (N·s−1)

0.50 527.74 (291.51) 526.28 (249.82) 0.99 312.01 (187.02) 407.47 (207.47) 0.39

0.10 535.89 (268.08) 541.07 (219.77) 0.96 343.61 (195.09) 423.99 (234.23) 0.49

0.20 477.22 (171.55) 491.10 (165.70) 0.85 352.22 (208.91) 384.68 (272.23) 0.74

Force (N)

Extension 205.87 (47.99) 223.55 (42.59) 0.05∗ 217.33 (49.60) 239.09 (63.03) 0.14

Flexion 111.95 (10.96) 125.56 (24.78) 0.23 121.41 (30.33) 123.66 (36.45) 0.76

RFD: rate of force development; TG: training group; CG: control group.∗Significant at paired student t-test.

1.50 m ± 0.64 for CG and TG), and weight (66.41 kg ± 9.55and 61.71 kg ± 4.55 for CG and TG) at baseline. Also, nodifferences were found on the physical activity level betweengroups before PNF program (6.85 ± 4.94 and 7.07 ± 2.74for CG and TG—P = 0.91). No differences were also foundbetween groups on the total BBS score at baseline; however,a significant training effect was found (P < 0.01) betweenBefore and after for TG (Table 2). The only activities thatwere different on After in comparison to Before for TGwere the “standing to sitting,” “standing with feet together,”“reaching forward with outstretched arm,” and “standingwith one foot in front” (P < 0.03), while no differences wereobserved for CG. Therefore, at After, all subjects on the TGachieved the maximal score on five of fourteen activities,while all volunteers on CG were successful to reach a perfectscore just on two of fourteen activities (the same result asBefore).

PNF program influenced in a positive way the maximalknee extensor torque for TG (P = 0.05) while no differences

were found for CG (Table 3). In the same way, no differenceswere found on knee flexor torque for both CG and TG afterthe program period (Table 3). No differences were also seenon rate of force development (Table 2) after the ten weeksperiod for TG and CG (P > 0.42).

Figures 2 and 3 present the VL, RF, VM, and BF neuro-muscular activation level during knee extension and flexioncontraction, respectively. No difference were observed forany muscles on both groups during knee isometric contrac-tions (P > 0.06). As seen on activation level, no differenceswere observed after PNF program on the coactivation indexaround the knee for TG (Before: 52.55 ± 17.46µV; After:53.00 ± 22.28µV). Also, the activation level in CG has notchanged (Before: 50.58± 15.01µV; After: 57.64± 11.50µV).

4. Discussion

The main result observed on results is that balance improvedaround 20% on training group after the PNF training,


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Figure 2: Mean (SD) knee muscles activation level during extension contraction.

while no differences were found for CG after this period.However, another interesting finding was that both rate offorce development and neuromuscular variables were notinfluenced by this program. Some explanations could beattributed to this lack of response to PNF program on thesevariables. (i) PNF does not result in adaptations on musclesfibers adaptations, as already found by others [17]. Hence,since rate of force development is direct related to musclefibers composition [10] this result was not unexpected. (ii)the effect of training programs on rate of force developmentwas attributed to neuromuscular adaptations, as the increasein the motor neuron recruitment level [10]. Since we foundno EMG differences between before and after 10 weeks(Figures 2 and 3), this could explain our lack of results onRFD. This data is also in agreement with other studies, whichhave shown that elderly do not increase their RFD afterstrengthening training [8].

The lack of neuromuscular response to PNF programcould be first attributed to the idea that test condition (iso-metric contraction on single plain) was not similar to exer-cises patterns (diagonal movements) and, therefore, results

could not be observed due to training type specificity[24]. It could be speculated that pre- and post-evaluationsshould be performed on the same exercises movementpatterns. However, the intention of this study was to simulateevaluations normally conducted on clinical day-life and theseinvolve strength tests performed on single movement planes.

Beside the lack of neuromuscular variables response,knee extension strength was positively affected by PNF pro-gram. Coactivation reduction could be responsible to explaina strength increase without neuromuscular response [25].However, as coactivation was also not influenced by PNFprogram (Table 3 and Figure 3), this last theory is unaccept-able. According to Jesper [26], in some conditions, strengthimprovement can be attributed to supraspinal neural adap-tations and not to peripheral paths, as normally seen. There-fore, since PNF exercises enhance proprioceptive response[17] and therefore promotes higher neural excitement levelon cortex [27], the training characteristics seem to beresponsible to explain the strength improvements observedon this study. However, this is only an assumption, since noevidences were investigated on this study to properly affirm


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Figure 3: Mean (SD) knee muscles activation level during flexion contraction.

that. Another explanation, obviously more plausible, is thatour training program improved proprioception, which couldexplain both the improvement on balance and knee exten-sion strength without neuromuscular response. However, wefailed to investigate directly proprioceptive variables as theposition sense.

However, our results let us to affirm that exercise pro-grams involving limb movements which follow diagonalmovement patterns, parallel to muscular topography andsimilar to that used on day-life activities can prepare subjectsto respond in a more properly way to balance [26] disturban-ces. We can affirm that, since we found higher Berg BalanceScale scores on TG, without response on CG. This result ishighly important to elderly, since they are more prone to fallsepisodes that can lead to an increase in mortality and finan-cial expenses.

Hence, it is also suitable to affirm that PNF trainingprogram used in this study induce a response more relatedto an appropriate reaction to balance perturbation than tostrength level improve. This is confirmed when PNF trainingresponse to individual tasks on Berg Balance Scale wereaccessed (Table 2). A higher performance after training

was achieved on activities where balance were perturbed,as standing with feet together, standing with one foot infront and reaching forward with outstretched arm, bothstatistically different when comparing Before versus After(Table 2). However, when tasks that involve strength wereanalyzed, as sitting to standing or placing alternate footon stool, no differences were found between Before versusAfter. Therefore, it is suggested that in future studies, theeffect of PNF should be tested on dynamic conditions asgait. This is a clear study limitation. Also, the low numberof subjects investigated in this study should be consideredas a study limitation. We could not discard the Hawthorneeffect and also it is not possible to affirm properly that PNFimplies in higher effects than other exercises methods, sinceno comparisons were conducted. However, this was not theobjective of this study and therefore it is suggested that futureinvestigations consider this topic.

An expressive improvement on fall risk in elderly aftera proprioceptive neuromuscular facilitation program wereseen in the present study, since volunteers presented a higherBerg Balance Scale performance and a higher knee extensorstrength level after training. Also, proprioceptive integration


or others central modulation processes and not peripheraladaptations are suggested to be responsible to such results,since no training effect were seen on both electromyographicvariables and knee extensor rate of force development.

Acknowledgment

This paper is supported by Fundacao de Amparo a Pesquisado Estado de Sao Paulo: FAPESP.

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